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12-2011
Have Introduced Brown Trout (Salmo Trutta)
Affected Native Aquatic Vertebrates in Western
United States Streams?
Nora K. Burbank
Utah State University
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HAVE INTRODUCED BROWN TROUT (SALMO TRUTTA) AFFECTED NATIVE
AQUATIC VERTEBRATES IN WESTERN UNITED STATES STREAMS?
by
Nora K. Burbank
A thesis submitted in partial fulfillment
of the requirements for the degree
of
MASTER OF SCIENCE
in
Ecology
Approved:
______________________________
Charles Hawkins
Major Professor
______________________________
Phaedra Budy
Committee Member
______________________________
David Koons
Committee Member
______________________________
Mark R. McLellan
Vice President of Research and
Dean of the School of Graduate Studies
UTAH STATE UNIVERSITY
Logan, Utah
2011
ii
2011Copyright © Nora Burbank 2011
All Rights Reserved
iii
ABSTRACT
Have Introduced Brown Trout (Salmo Trutta) Affected Native Aquatic Vertebrates
in Western United States Streams?
by
Nora Burbank, Master of Science
Utah State University, 2011
Major Professor: Dr. Charles Hawkins
Department: Watershed Sciences
The introduction of exotic species is one of the greatest threats to freshwater
biodiversity. Brown trout are native to Eurasia, but have been introduced to much of the
rest of the world, including the United States. In other parts of their introduced range,
brown trout have caused substantial negative effects to native species‟ abundances and
distributions, and have altered the structure of some aquatic communities. In the United
States, studies of some streams and watersheds have shown that brown trout can
negatively affect native species, but I found no study that considers the effect of brown
trout across a large portion of their introduced range.
For this study, I examined if (1) the abundance and distribution of two
ecologically different native fish taxa (sculpins and speckled dace) and (2) the structure
of entire stream vertebrate assemblages were negatively associated with the presence and
abundance of brown trout. I based my analyses on existing, standardized survey data
iv
collected across streams of the western United States. I found no relationship between
brown trout and the abundance, presence-absence, or probability of detection of sculpins
or speckled dace. I also found that brown trout were not associated with the structure of
native stream vertebrate assemblages. My results imply that native stream vertebrates in
western US streams are able to coexist with brown trout across the western United States,
despite the negative effects brown trout can have on some taxa in individual watersheds
or rivers.
(58 pages)
v
PUBLIC ABSTRACT
Have Introduced Brown Trout (Salmo Trutta) Affected Native Aquatic Vertebrates
in Western United States Streams?
by
Nora Burbank, Master of Science
Utah State University, 2011
Major Professor: Dr. Charles Hawkins
Department: Watershed Sciences
The introduction of exotic species to areas outside of their native range is one of
the greatest threats to the biodiversity of native freshwater organisms. Exotic species
have outcompeted native species for resources such as food and shelter, and in some
cases these interactions have resulted in local extinctions or reductions in abundance of
those native species. Brown trout are native to Eurasia, but have been introduced to
much of the rest of the world, including the United States. In some parts of their
introduced range, brown trout have substantially reduced the abundance and home ranges
of some native fish species. In the United States, brown trout have been intentionally
stocked in many streams and rivers across the country because they are a desirable sport
fish. A few studies have shown that these fish negatively affect some native fish species.
However, I found no studies that considered the effect of brown trout on native species
across a large portion of their range in the United States.
vi
For my thesis, I examined if the presence and abundance of brown trout have
affected (1) the abundance, presence, and distribution of two ecologically different native
fish taxa (sculpins and speckled dace) and (2) the composition and relative abundances of
entire assemblages of native stream vertebrates in streams across 12 western United
States. I found no relationship between brown trout and the abundance, presence or
absence, or distribution of either sculpins or speckled dace. I also found that brown trout
were not associated with differences in the composition of the native stream vertebrate
assemblages. My results imply that native stream vertebrates are able to successfully
coexist with brown trout across the western United States, and therefore may not
experience the extreme changes in abundance or distribution that some exotic species
may cause.
vii
ACKNOWLEDGMENTS
I am very fortunate to have Dr. Charles Hawkins as my major professor, whose
guidance and support have made me a better researcher. My committee members, Dr.
Phaedra Budy and Dr. David Koons, provided insightful and helpful comments and
suggestions during all stages of my study. Ryan Hill and John Olson were immensely
supportive and helpful, and I am eternally grateful for their friendship and support. Brian
Creutzburg, Ellen Wakeley, and Jake Vander Laan all provided helpful advice and
insightful comments. Gary Thiede and Peter MacKinnon were very helpful during the
experiment that shall not be named. I also want to thank my family and friends,
especially Ian Washbourne, for their support.
Nora Burbank
viii
CONTENTS
Page
ABSTRACT .................................................................................................................. iii
PUBLIC ABSTRACT ..................................................................................................... v
ACKNOWLEDGMENTS .............................................................................................vii
LIST OF TABLES .......................................................................................................... x
LIST OF FIGURES ........................................................................................................xi
CHAPTER
I. INTRODUCTION ............................................................................................... 1
Definition of problem ..................................................................................... 6
II. METHODS ........................................................................................................ 10
Study area and data ...................................................................................... 10
Habitat variables .......................................................................................... 11
Reduced datasets .......................................................................................... 13
Sculpins ....................................................................................................... 14
Speckled dace............................................................................................... 15
Niche overlap with brown trout .................................................................... 16
Brown trout and the abundance and
presence-absence of target taxa.................................................................. 16
Niche models for target taxa ......................................................................... 17
Relationship between assemblage groups
and brown trout ......................................................................................... 18
III. RESULTS .......................................................................................................... 20
Brown trout and the abundance and
occurrence of the target taxa ...................................................................... 20
Brown trout and the target taxa niche
models ....................................................................................................... 20
Assemblage structure analysis ...................................................................... 24
ix
IV. DISCUSSION .................................................................................................... 28
V. CONCLUSIONS ............................................................................................... 35
VI. REFERENCES .................................................................................................. 39
x
LIST OF TABLES
Table
Page
1
Description of the 18 habitat variables used in the principal components analysis,
random forests models, and PERMANOVA analysis. EMAP variables and
descriptions can be viewed and downloaded from http://www.epa.gov/wed/pages/
models/EMAP_West_Data.htm; PRISM variables can be viewed and downloaded
from http://www.prism.oregonstate.edu/; STATSGO variables can be viewed and
downloaded from http://soils.usda.gov/survey/geography/statsgo/. ...................... 12
2
Results of the two-sample t-tests on sculpin and speckled dace abundances
including means (log10number/m), standard deviations (s.d.), number of sites (n),
and p values. ........................................................................................................ 21
3
2x2 contingency tables used to test the dependence of sculpin (a) and speckled
dace (b) presence or absence on brown trout presence or absence. Chi square tests
were not significant for either sculpin (p=0.17) or speckled dace (p=0.80). .......... 21
4
Measures of prediction accuracy for the sculpin and speckled dace random forest
models. ................................................................................................................ 21
5
Prevalence of each species in each of the assemblage groups derived from the
cluster analysis. ................................................................................................... 26
6
Sources used to construct Figure 8. .................................................................... 33
xi
LIST OF FIGURES
Figure
Page
1
Conceptual framework outlining the invasion process. ......................................... 5
2
Locations of all 776 EMAP sample sites across the western United States. Black
dots indicate sites where brown trout were captured. .......................................... 11
3
Scatterplots demonstrating the overlap in niche space between brown trout (open
circles) and sculpins and speckled dace (black dots) as defined by PCA Factors 1
and 2. ................................................................................................................. 17
4
Variable importance plots for the predictor variables from the random forests
models for sculpins and speckled dace. A higher mean decrease in accuracy
indicates greater error when the variable is excluded from the model. ................ 22
5
Partial dependence plots for the probability of detection for sculpins based on all
predictor variables after averaging out the effects of the other predictor variables
in the model. ...................................................................................................... 23
6
Partial dependence plots for the probability of detection for speckled dace based
on all predictor variables after averaging out the effects of the other predictor
variables in the model. ....................................................................................... 25
7
Locations of sites assigned to each of the six assemblage groups. ....................... 27
8
Conceptual representation of the variable effects of brown trout on native fishes.
A small effect was inferred when a study did not detect any measureable effect, a
moderate effect (marked by the vertical line) was inferred as a measurable change
that still allowed the species to coexist with brown trout (in growth, habitat or diet
selection), and a large effect was inferred as a change in growth or survival that
makes coexistence with brown trout difficult or not possible. Benthic taxa are
shown in bold font, and water column species are shown in italics. Superscripts
refer to the type of interaction: apredation, bcompetition, and cother. One species
(*) was introduced to the native range of brown trout. Subscripts identify the
sources of information, which are given in Table 6............................................. 32
CHAPTER I
INTRODUCTION
Biological invasions are one of the greatest threats to biodiversity and the
persistence of threatened species (Allan and Flecker 1993; Sakai et al. 2001; Dudgeon et
al. 2006), and the widespread introduction of exotic species into freshwaters is considered
one of the greatest threats to these ecosystems (Dudgeon et al. 2006). Exotic fishes may
be introduced by humans unintentionally through accidental releases or intentionally
through stocking for either recreation or as biological controls of pest species (Lockwood
et al. 2007; Gozlan et al. 2010). Exotic species are often novel predators and competitors
in the ecosystems to which they are introduced, and they can be especially threatening
because native species often lack the behaviors and adaptations necessary to avoid harm.
For example, introduction of piscivorous Nile Perch (Lates niloticus) to Lake Victoria
contributed to massive declines and extinctions of over 200 endemic cichlid species
(Goldschmidt et al. 1993; Kitchell et al. 1997). Two common themes exist in the
literature regarding the invasion process and the effects of exotic species on native
ecosystems. The first is that the effect of the introduction of new species on the receiving
ecosystem is variable. Second, the invasion of an exotic species into a new area is a
stepwise process that begins with establishment and can end with major impact.
Species invasions are common although the effects of these species on the native
ecosystem are variable. Williamson (1996) argues that of all the species introductions
that occur, only 10% will result in successful establishment in the new habitat; and only
10% of those will result in severe negative effects on the receiving ecosystem, a
2
contention that is supported by other authors (Lodge 1993; Simberloff 2007; but see
Jeschke and Strayer 2005 for a contrasting view). Therefore, it is important to understand
not only the process by which successful invasions occur, but also the processes that
hinder successful invasions.
The invasion of a species into a new area is a stepwise process that begins with
initial introduction and has variable end stages (e.g. Williamson 1996; Shea and Chesson
2002; Lockwood 2007; Nentwig 2007). Different authors emphasize different steps as
important in their conceptual frameworks of the invasion process. For example, Shea and
Chesson (2002) argue that there are two stages of the invasion process: 1) transport of the
species to the new area, and 2) establishment and population increase in that new area.
Alternatively, Williamson (1996) posits that there are four main stages in the invasion
process: arrival and establishment, spread, population equilibrium, and effect on the
native ecosystem.
From a management perspective, a useful conceptual framework of the invasion
process includes establishment in the new area, interactions with the native ecosystem,
and effects on the native ecosystem (Figure 1). Interactions with the native ecosystem
are differentiated from major negative effects because while all introduced species will
interact with the receiving ecosystem, not all will cause severe negative ecological or
economic effects (Williamson 1996; Simberloff 2007). It is important to identify the
effect that the introduced species is having on the receiving ecosystem to effectively
manage the introduced species and native ecosystem.
3
Following initial introduction, the first step in the invasion process is
establishment in the new area, which occurs if the introduced species forms a selfsustaining population that persists by natural reproduction (Gozlan et al. 2010). The
reason few introductions result in establishment is likely associated with the specific
factors, both abiotic and biotic, that affect habitat suitability. Once established, the
introduced species may also spread to new areas, and become established at those places.
Spread can be natural, but is often facilitated by human activities, such as stocking for
recreational purposes, such as angling (Taylor et al. 1984).
Although we do not completely understand the relative influence of biotic and
abiotic factors in allowing exotic species establishment (Moyle and Light 1996), it is
widely recognized that aspects of both the receiving environment and community are
important. For establishment to occur, the receiving environment must be suitable for the
survival of all life stages, and sufficient food resources must be available (Townsend
1996). Within areas of suitable environmental conditions, some aspects of the receiving
community may facilitate establishment. For example, introduced species are more
likely to become established in locations that do not already contain potential predators or
strong competitors (Townsend 1996; Sakai 2001). Additionally, members of speciespoor communities are thought to be maladapted to multiple predators and competitors,
thus making these communities more susceptible to invasion (Lodge 1993; Townsend
1996).
Successful invaders often possess several common biological and ecological
traits. First, large founding population size appears to promote successful establishment,
4
especially given multiple introduction attempts (Williamson 1996; Kolar and Lodge
2001). Species with wide native environmental or geographic ranges are thought to be
more successful invaders because of a presumed wide tolerance of multiple different
habitat conditions (Townsend 1996). Lawton and Brown (1986) also observed a positive
correlation between body size and establishment success of vertebrates, which may be
due to the fact that larger animals tend to have fewer predators (Townsend 1996).
Animals with broad food niches also tend to be successful invaders, as do those with a
high reproductive output and multiple reproductive events per female (Townsend 1996).
Once established, introduced species may interact with the receiving ecosystem in
several ways. Exotic species may introduce new parasites and diseases, hybridize with
natives (which can reduce fitness of native species), and compete with or predate on
natives (Taylor et al. 1984). These interactions may not always be negative, or may be
relatively minor, allowing native taxa to coexist with the introduced species. For
example, Nasmith et al. (2010) studied the effect of stocked non-native trout on native
fish in several lakes in Alberta, Canada. Dace (Phoxinus spp.) altered their feeding
behavior in the presence of trout, and their size structure in stocked lakes was consistent
with size limited predation. However, these effects did not result in any detectable
change in the abundance of the dace, prompting the authors to conclude that the stocking
of trout can be compatible with the persistence of healthy native fish populations. Thus,
some introduced species are able to coexist with native species without causing major
negative effects.
5
Figure 1. Conceptual framework outlining the invasion process.
6
In the context of native species conservation, it is important to differentiate
between interactions and subsequent effects that allow native species to coexist with
introduced species (such as those outlined in the above section) and those that do not
allow for coexistence (such as extirpations or substantial reductions in abundance).
Population and individual growth rates, abundance, distribution, behavior, and species
richness and diversity are commonly measured in studies that assess the potential effect
of introduced species on native individuals and communities (Lodge 1993; Williamson
1996; Parker et al. 1999).
Definition of problem
In the United States, freshwater fauna have shown alarmingly high rates of
extinction (Miller et al. 1989; Taylor et al. 1996; Ricciardi and Rasmusen 1999) and
increasing rates of imperilment (Lannoo 2005; Jelks et al. 2008) over the last century.
Threats to freshwater fauna include habitat alteration and destruction, pollution, flow
modification, but the introduction of exotic species presents a particularly important
threat because once an exotic species has successfully established, there is little hope for
eradication (Allan 1995; Richter 1997; Dudgeon et al. 2006).
Brown trout (Salmo trutta) are native to Eurasia, but because they are a valued
sportfish have become widely established outside of their native range. They are such a
successful invader that the World Conservation Union considers them to be one of the
world‟s 30 worst invasive species (McIntosh et al. 2011). They possess many of the
biological and ecological attributes that facilitate long-term survival in a new location,
7
such as a wide native range that includes a variety of suitable habitats, a generalist diet, a
high reproductive output (e.g. up to 7,500 eggs per female; Becker 1983), and multiple
reproductive events per female (Elliot 1994; Townsend 1996). These characteristics,
combined with extensive stocking efforts, have facilitated the widespread introduction
and establishment of brown trout in at least 29 countries outside of their native range
(McIntosh et al. 2011). Brown trout are aggressive predators (Nillson 1963) that can
negatively affect native fauna within their introduced range. Predation by introduced
salmonids, including brown trout, has been implicated as a major cause of a decline in
some native fishes (family Galaxiidae) in New Zealand (Townsend and Crowl 1991;
McIntosh et al. 2010). Additionally, introduced salmonids, including brown trout, have
become a majority component of the overall fish biomass and abundance in many
Chilean streams (Soto et al. 2006; Arismendi et al. 2009). Native fish were not found in
40% of streams surveyed by Soto et al. (2006), and Arismendi et al. (2009) concluded
that predation by introduced salmonids, including brown trout, caused a decline in the
abundance of native fishes in six Chilean lakes.
Brown trout were first introduced to the United States in 1883, and through
extensive stocking efforts have since become naturalized throughout most of the country
(Becker 1983; Behnke 2002). In streams of the western United States, brown trout are
now among the most widely distributed and abundant nonnative aquatic vertebrate
species and have become incorporated into resident fish assemblages (Schade and Bonar
2005; Lomnicky et al. 2007). Despite their widespread distribution, the study of the
effect of brown trout on native fishes is relatively new - about 15 years (McIntosh et al.
8
2011). Brown trout are partially piscivorous in the United States (Hannuksela 1969;
Stauffer 1977; He and Wurtsbaugh 1993), and considered superior competitors to some
native fishes (McHugh and Budy 2005, 2006; Wang and White 1994). Brown trout have
also been associated with reduced growth and abundance of some North American native
fish species (Garman and Nielsen 1982; Zimmermann and Vondracek 2006), and have
replaced native brook trout (Salvelinus fontinalis) in many streams of eastern North
America (Waters 1983; Sorensen et al. 1995; Grant et al. 2002). Additionally, mountain
yellow-legged frogs (Rana mucosa) in California are negatively associated with
introduced trout, including brown trout (Knapp and Matthews 2000). These
observations, coupled with their widespread distribution, known piscivory in the United
States, and consistent negative associations with native fauna elsewhere, suggest that
brown trout may be profoundly affecting native aquatic vertebrates across the western
United States.
Our objective was to determine how severely brown trout have affected the
abundance and distribution of native aquatic vertebrates in streams of the western United
States. We approached this study in two ways. First, we used survey data to determine if
the abundance and occurrence of two common native taxa, sculpins (Cottus spp.) and
speckled dace (Rhinichthys osculus), were negatively associated with brown trout
occurrence and abundance. These taxa differ in their life histories, behavioral ecology,
and geographic distribution, but both are native to streams now occupied by brown trout
(see Sculpins and Speckled dace below). For both taxa, we hypothesized that their
abundances and probabilities of detection would be smaller at sites that contained brown
9
trout. Second, we tested the hypothesis that the structure of entire native aquatic
vertebrate assemblages differs between streams with and without brown trout.
10
CHAPTER II
METHODS
Study area and data
The study area included 12 states in the western United States (Figure 2). We
used aquatic vertebrate data collected from perennial streams and rivers by the United
States Environmental Protection Agency‟s Environmental Monitoring and Assessment
Western Pilot Project (EMAP). The EMAP project used a probabilistic site selection
design and sampled a total of 1,361 sites in streams and rivers to characterize aquatic
vertebrate assemblages and their associated local habitat characteristics within the study
area (Figure 2; Stoddard et al. 2005; Lomnicky et al. 2007). For each of these sites, the
EMAP project recorded the completeness of the vertebrate sample as „Failed‟,
„Insufficient‟, „Yes-partial‟, or „Yes-all‟. To maximize sample comparability, we only
used sites recorded as „Yes-all,‟ resulting in a data set of 776 sites. A total of 136 native
species were observed at these 776 sites, and counts were available for each species at
each site. The species collected were predominantly fish (80%).
Habitat variables
For both the taxon-specific and assemblage-level analyses, we used candidate
predictor variables that described physical and climate conditions at each site. The
EMAP project collected a suite of habitat variables at each site, and we used 11 of these
variables in our analyses (Table 1). In addition to the EMAP variables, we used PRISM
climate data (Daly et al. 2000) and STATSGO soils data (Wolock 1997) to calculate 7
11
additional predictor variables that described precipitation and air temperature for each
site‟s watershed (Table 1). These variables were considered because air temperature is
strongly correlated with stream temperature (Mohseni et al. 1998), and fish distributions
are often strongly associated with climate conditions (Heino 2002; Buisson et al. 2008;
Griffiths 2010). Climate factors are also frequently used to describe and predict the
suitability of fish habitat (Eaton and Scheller 1996; Rahel et al. 1996; Steen et al. 2010).
Figure 2. Locations of all 776 EMAP sample sites across the western United States.
Black dots indicate sites where brown trout were captured.
12
Table 1. Description of the 18 habitat variables used in the principal components
analysis, random forests models, and PERMANOVA analysis. EMAP variables and
descriptions can be viewed and downloaded from
http://www.epa.gov/wed/pages/models/EMAP_West_Data.htm; PRISM variables can be
viewed and downloaded from http://www.prism.oregonstate.edu/; STATSGO variables
can be viewed and downloaded from http://soils.usda.gov/survey/geography/statsgo/.
Variable
bankful width
bed particle
diameter
elevation
fast habitat
full cover
organic matter
sand and fines
slope
substrate diameter
width
width*depth
width/depth
woody and
vegetation cover
max temp
Unit
m
mm
m
%
fraction
of
reach
%
%
%
mm
m
m2
m/m
cover
°C
mean precip
mm
mean temp
°C
min precip
mm
min temp
°C
water table depth
m
Description
Mean bankful stream width
Estimate of critical bed particle diameter at
bankful stage
Elevation at center of reach (m)
% Fast water habitat (riffle and faster)
Ground, mid-canopy and canopy cover
present
Source
EMAP
EMAP
% Substrate as wood or detritus
% Substrate ≤ 16mm
Mean channel slope
Mean streambed particle diameter
Mean wetted width (m)
Mean width*depth product
Mean channel width-depth ratio
Riparian vegetation canopy cover + mid
layer woody cover
Mean 1971-2000 annual maximum
monthly air temperature for the watershed
Mean 1971-2000 average annual
precipitation values for the watershed
Mean 1971-2000 annual average monthly
air temperature for the watershed
Mean 1971-2000 minimum annual
precipitation values for the watershed
Mean 1971-2000 annual minimum
monthly air temperature for the watershed
Average depth to water table
EMAP
EMAP
EMAP
EMAP
EMAP
EMAP
EMAP
EMAP
EMAP
EMAP
EMAP
PRISM
PRISM
PRISM
PRISM
PRISM
STATSGO
13
Reduced datasets
Because brown trout are an introduced species, non-detections can represent
absences caused by unsuitable habitat, locations where brown trout have not been
introduced or established, or sampling error (i.e. a failure to detect their occurrence).
Additionally, because brown trout continue to be stocked in the western United States,
the detection of brown trout may not represent suitable conditions for brown trout
establishment and long-term success. We therefore, restricted our analyses to only sites
that had a high potential of being suitable habitat for brown trout. To identify suitable
brown trout habitat, we used principal components analysis (PCA) to characterize the
environments used by brown trout based on five environmental variables: elevation, longterm mean maximum and mean minimum annual air temperature of the watershed,
channel slope and channel width (Table 1). Preliminary analyses demonstrated that these
five variables were predictive of brown trout occurrence. Prior to analysis, we checked
all variables for approximate normality by inspecting normal probability plots. Channel
width was the only variable that required transformation (log 10(x+1)). The PCA
identified three main axes of habitat variation. These axes were associated with elevation
and maximum air temperature (Factor 1), minimum air temperature and channel slope
(Factor 2), and channel width (Factor 3). We then used the 102 sites where brown trout
were collected to estimate habitat conditions that were likely to be highly suitable,
defined here as those sites with factor scores between the 10th and 90th percentiles of
factor score values associated with the 102 brown trout presences. This analysis
identified 173 sites with a high potential for suitable brown trout habitat, 51 at which
14
brown trout were observed. This screening eliminated 50% of the sites where brown
trout occurred, but should have identified those sites most likely to support established
brown trout populations.
We also restricted our analyses to those sites that the native taxa could also
potentially inhabit. To identify these sites, we selected sites from the 173 candidate sites
described above that fell within the geographic range of each of the two target taxa. We
defined the geographic range of native taxa to include any USGS sub region (Saber et al.
1987) that contained at least one site where the native taxon had been reported. These
restrictions resulted in two separate datasets, one for sculpins (n=109 sites, hereafter the
sculpin dataset) and another for speckled dace (n=110 sites, hereafter the speckled dace
dataset).
Sculpins
Sculpins were widely distributed in the EMAP dataset, and occurred in 122 of the
776 sites. Sculpins are morphologically adapted to benthic environments (e.g. lack of a
swim bladder; Fänge 1966), are predators that mainly consume benthic invertebrates but
will also consume fish and fish eggs (Fitzsimons et al. 2006), and typically occur in cold
waters across North America (maximum tolerable temperature 24.3°C; Eaton and
Scheller 1996). We used genus-level data in our analyses because different species have
generally similar habitat preferences and feeding strategies and many individuals in the
dataset were only identified to genus. In addition, the taxonomy of sculpins is uncertain
and there are likely many more individual species than are currently described (Kinziger
15
et al. 2007). Sculpins are often sympatric with brown trout in North America (Bailey
1952; Brown and Downhower 1982; Quist et al. 2004). Few studies have examined
interactions between sculpins and brown trout, but brown trout are known predators of
mottled sculpin in the Logan River, Utah (Wood 2008) and are an assumed prey item of
brown trout in Lake Ontario, Canada (Jones et al. 1993; Jackson 1997).
Speckled dace
Speckled dace are native to streams and rivers of the western United States and
have a wide geographic distribution. Speckled dace are habitat generalists and are found
in habitats ranging from small creeks and isolated springs to rivers and in biomes ranging
from deserts to mountains, but they prefer cool to cold water (Sigler and Sigler 1987;
Moyle 2002). Within their native range, speckled dace often occur in streams and
watersheds suitable for brown trout (Holden and Stalnaker 1975; Lanigan and Berry
1981; Erman 1986; Quist et al. 2004), and brown trout are a known predator of speckled
dace in the Little Colorado River, AZ (Marsh and Douglas 1997). With the exception of
Marsh and Douglas (1997), we are aware of no other studies that have documented
interactions between speckled dace and introduced brown trout. However, brown trout
predation is one proposed method for controlling populations of another dace-like
species, Phoxinus phoxinus, which was introduced in Norwegian lakes (Museth et al.
2003). Additionally, predation by introduced trout, including brown trout, is known to
negatively affect the growth and habitat use of dace (Phoxinus spp.) in several Canadian
16
lakes (Nasmith et al. 2010). The results of these studies suggest that brown trout have the
potential to negatively affect the abundance and distribution of speckled dace.
Niche overlap with brown trout
To ensure that the sites selected in the reduced datasets were suitable for both
brown trout and the native taxa, we qualitatively examined the overlap in observed niche
space between brown trout and the two target taxa. We used all sites from the full EMAP
dataset where sculpins were present, and examined the distribution of sites with and
without brown trout in principal component ordination space (PC factors 1 and 2). PCA
Factors 1 and 2 were selected because they contained the two temperature variables, and
temperature is a strong limiting factor for fish (Eaton et al. 1995). We conducted the
same analysis for speckled dace. The niche space of sculpins and brown trout almost
completely overlapped (Figure 3), and only a slight difference existed in the niche spaces
of brown trout and that of speckled dace (Figure 3).
Brown trout and the abundance and
presence-absence of target taxa
To assess the effect of brown trout on the abundance of sculpins and speckled
dace, we conducted two-sample t-tests on the abundances of the target taxa at sites where
brown trout were present and absent. We first standardized counts as number of fish (i.e.
sculpins or speckled dace) caught per meter of stream length. We transformed
(log10(x+1)) these values to meet assumptions of normality.
17
Figure 3. Scatterplots demonstrating the overlap in niche space between brown trout
(open circles) and sculpins and speckled dace (black dots) as defined by PCA Factors 1
and 2.
We determined if the presence of each target taxon was associated with the
presence of brown trout by testing if the frequencies of occurrence of the target taxa were
independent from the occurrence of brown trout (Chi-square test; Zar 1999).
Niche models for target taxa
We used Random Forest (RF) models („randomForest‟ package in R; R Core
Development Team 2010) to quantify relationships between the probability of detection
of the two target taxa and both brown trout counts (standardized as brown trout per meter
stream) and habitat predictors. RF models were evaluated based on five performance
metrics: percent sites correctly classified (PCC), sensitivity (the percent of presences
correctly classified), specificity (the percent of absences correctly classified), Cohen‟s
18
kappa (kappa), and the area under the receiver operating characteristic curve (AUC).
Cohen‟s kappa is a measure of the agreement between modeled predictions and
observations after chance agreement is accounted for, and ranges from -1 to +1, with +1
indicating perfect agreement and values ≤0 indicating no agreement better than chance
(Cohen 1960). AUC measures the ability of the model to discriminate between sites
where the species is present and sites where it is absent (Elith et al. 2006). The statistic
ranges from 0 to +1, with +1 indicating perfect discrimination. RF models are especially
useful in niche modeling because they capture non-liner and interactive relationships and
are difficult to overfit (Cutler et al. 2007). RF output includes a measure of the relative
importance of each of the predictor variables, and we used partial dependency plots
(Cutler et al. 2007) to depict how the modeled probabilities of detection of the target
species varied with each predictor after holding the effects of all other predictors
constant.
Relationship between assemblage groups
and brown trout
For the analysis of the association between native aquatic vertebrate assemblages
and brown trout we also restricted the data to include only those sites with potentially
suitable brown trout habitat. We defined assemblages as the native aquatic vertebrates,
primarily fishes, that collectively inhabit a stream reach. We identified groups of
biotically-similar sites by clustering (flexible beta UPGMA) sites based on similarity
(Sorensen index) in taxon presence-absences. Prior to clustering, we removed rare taxa
(<5 sites) because rare taxa generally produce noise in such analyses (McCune and Grace
19
2002). After selecting sites suitable for brown trout and removing rare taxa, the dataset
consisted of 132 sites containing 17 taxa; 16 fishes and the tailed frog, Ascaphus truei.
Brown trout were observed at 33 of these sites.
We used multivariate analysis of variance with permutations (PERMANOVA) to
determine if the structure of the six assemblage groups was associated with the presence
of brown trout. For each of the six assemblages, we tested if the assemblages observed at
the sites were significantly different in the presence and absence of brown trout. We used
the 'adonis' function in the vegan R statistical software package for this analysis (R Core
Development Team 2010).
20
CHAPTER III
RESULTS
Brown trout and the abundance and
occurrence of the target taxa
We found no relationship between brown trout presence and either the
abundance or occurrence of the target taxa. Neither the two-sample t-test based on the
abundances of the two target taxa (Table 2) nor the contingency table based on the
presence-absence of brown trout and the presence-absence of the two target taxa (Table
3) were significant.
Brown trout and the target taxa niche
models
Brown trout abundance was also not an important predictor of the probability of
detecting either target taxon. The RF models for the two target taxa had similar
performance, though they differed in the relative importance of habitat predictors (Table
4, Figure 4). Five habitat predictor variables were included in the final RF model for
sculpins: channel width, width to depth ratio, mean annual air temperature, minimum
annual air temperature, and percent of organic matter in the substrate (Figures 4 and 5,
Table 1). When brown trout abundance was included in the model it was the least
important predictor and did not improve model performance, as evident in its partial
dependence plot (Figure 5).
For speckled dace, eight habitat predictor variables were included in the final RF
model: mean annual precipitation, mean annual air temperature, maximum annual air
21
Table 2. Results of the two-sample t-tests on sculpin and speckled dace abundances
including means (log10number/m), standard deviations (s.d.), number of sites (n), and p
values.
Brown trout
No brown trout
Speckled Brown trout
dace
No brown trout
Sculpins
Mean
-1.47
-1.56
-1.95
-1.70
s.d.
1.1
0.9
0.8
0.9
n
27
82
31
79
p value
0.69
0.12
Table 3. 2x2 contingency tables used to test the dependence of sculpin (a) and speckled
dace (b) presence or absence on brown trout presence or absence. Chi square tests were
not significant for either sculpin (p=0.17) or speckled dace (p=0.80).
a)
Brown trout
Absent Present
Absent
42%
10%
Sculpins
Present
33%
15%
b)
Speckled Absent
dace
Present
Brown trout
Absent Present
53%
20%
19%
8%
Table 4. Measures of prediction accuracy for the sculpin and speckled dace random forest
models.
Specificity
Sensitivity
PCC (%)
Kappa
AUC
(%)
(%)
Sculpins
77
76
78
0.54
0.81
Speckled
dace
81
91
53
0.48
0.84
22
Figure 4. Variable importance plots for the predictor variables from the random forests
models for sculpins and speckled dace. A higher mean decrease in accuracy indicates
greater error when the variable is excluded from the model.
23
Figure 5. Partial dependence plots for the probability of detection for sculpins based on
all predictor variables after averaging out the effects of the other predictor variables in the
model.
24
temperature, mean width to depth ratio, bed particle diameter, riparian vegetation
composition, percent sand and fine particle substrate, and percent fast-water habitat
(Figure 4, Table 1). Brown trout abundance did not improve the performance of the
speckled dace model and was the least important predictor. The partial dependence plot
for speckled dace confirmed that there was no relationship between brown trout and the
probability of detection of speckled dace (Figure 6).
Assemblage structure analysis
From the cluster analysis, we visually identified six groups of taxa that were
associated with one another. The groups varied in terms of both species richness and
composition (Table 5), and showed modest spatial coherence (Figure 7). Group 1
consisted of sites typically found in southwestern, arid regions. Speckled dace was the
most frequently occurring species in this group. Group 3 consisted of sites found in the
high plains east of the Rocky Mountains, and longnose dace (Rhinichthys cataractae) and
white sucker (Catostomus commersoni) were the two most common species in this group.
Group 4 consisted of sites in high-elevation streams, and cutthroat trout (Oncorhynchus
clarkii) was the most prevalent species in this group, occurring at all sites. Groups 2 and
6 consisted of sites widely distributed in mountainous areas, and cutthroat and rainbow
trout were the most common species in these two groups, respectively. Group 5 also
consisted of sites in mountainous areas, and mottled sculpin (Cottus bairdii) occurred at
all of these sites.
25
Brown trout occurred in at least two sites in all six groups, with a similar
prevalence (0.22-0.33) in Groups 1-3, 5 and 6, and a lower prevalence (0.13) in Group 4
(Table 5). No relationship was detected between brown trout counts and variation in
taxonomic composition among assemblage groups (p = 0.29).
Figure 6. Partial dependence plots for the probability of detection for speckled dace based
on all predictor variables after averaging out the effects of the other predictor variables in
the model.
26
Table 5. Prevalence of each species in each of the assemblage groups derived from the
cluster analysis.
Group and number of sites
1
2
3
4
5
6
Species
(27)
(18)
(13)
(16)
(12)
(46)
Brown trout
0.30
0.22
0.31
0.13
0.33
0.24
Creek chub
0
0
0.46
0
0
0
Cutthroat trout
0
0.39
0
1.00
0.67
0.24
Desert sucker
0.19
0
0
0
0
0
Fathead minnow
0.07
0.06
0.23
0
0
0
Longnose dace
0
0.06
0.85
0
0.17
0.02
Longnose sucker
0
0
0.23
0
0.08
0.07
Mottled sculpin
0
0.06
0
0
1.00
0.28
Mountain sucker
0.11
0.17
0.31
0
0.17
0.02
0
0.06
0.08
0.06
0.17
0.07
Paiute sculpin
0.11
0
0
0.13
0
0.07
Rainbow trout
0.33
0.28
0.15
0
0
1.00
Redside shiner
0.11
0.11
0
0
0
0
0
0.28
0
0
0
0.04
1.00
0.06
0
0
0.17
0
Tailed frog
0
0.28
0
0
0.08
0.11
Utah sucker
0.04
0.17
0
0
0.17
0
White sucker
0
0
0.77
0
0
0
Mountain whitefish
Shorthead sculpin
Speckled dace
27
Figure 7. Locations of sites assigned to each of the six assemblage groups.
28
CHAPTER IV
DISCUSSION
Considerable research has been conducted worldwide that analyzes the effect of
introduced brown trout on native fishes, indicating that there is general concern about the
possible negative effects of these predators. The results of our study stand in marked
contrast to that view and the conclusions drawn from several other studies. There are
several possible explanations for the lack of associations in our study. First, our study
design and analyses may have been incapable of detecting real effects (i.e. the design or
analyses produced type II errors of inference). Second, the severity of effects of brown
trout on native fauna may be dependent on other factors that mitigated potentially
negative effects in western United States streams. Finally, native aquatic vertebrates in
the western United States may be less susceptible to predation and competition by brown
trout than in previously studied systems.
We do not think that the design of our study or our analyses suffered from larger
Type II errors than occurred in previous studies. Although the data were not collected
specifically to assess effects of brown trout, they spanned a wide range of abiotic and
biotic conditions. In addition, the site selection criteria used by the EMAP project made
the dataset robust to the statistical analyses that we used. Electrofishing was the primary
fish sampling technique used by EMAP project crews, and sein nets were rarely used.
Small fish, such as sculpins and speckled dace, are not as effectively captured by
electrofishing as larger bodied fish, which probably resulted in underestimates of the
29
counts of such fish at each site. However, any bias introduced by sampling methods
should have been consistent across sites, thus making comparisons between sites valid.
The strength of the effect of brown trout on other native species has been shown to be
dependent on interactions between multiple variables (McIntosh 2000) which could have
obscured negative effects. However, the RF analysis should have detected such
interactions (Cutler et al. 2007), but inspection of the bivariate partial dependence plots
showed no interaction between brown trout counts and other predictor variables on the
detection of the two target taxa.
Instead of errors in study design and analyses, we think a more likely explanation
for the observed lack of association is that native aquatic vertebrate species in the western
United States possess behaviors and other adaptations that better allow them to coexist
with brown trout than native taxa in other regions. Introduced species are thought to have
the greatest effects when they represent an entirely novel member of the community
(Ruesink et al. 1995; Parker et al. 1999). Native aquatic vertebrates in the western United
States have coevolved alongside other piscivorous salmonids (e.g. cutthroat and rainbow
trout), and currently coexist with those species. Thus, although brown trout are known
predators of many native aquatic vertebrates, their establishment may not represent a
significantly novel stress. Much of the evidence that implicates brown trout as a threat to
native fauna comes from studies conducted in New Zealand, which, prior to the
introduction of brown and rainbow trout, lacked any salmonid-type piscivore (McDowall
2006).
Co-occurrence within the sample reaches may also have been facilitated if native
30
taxa and brown trout used different habitats within those reaches. For example, native
brown trout and Siberian sculpin (Cottus poecilopus) occupy different microhabitats in
stream reaches that both inhabit (Hesthagen and Heggenes 2003; Hesthagen et al. 2004).
Therefore, although the two species coexisted in the same stream reach, their
microhabitat preferences may limit the opportunities for interactions between the two. A
separation of microhabitat use is especially pronounced between brown trout and benthic
species, such as sculpins, because brown trout are primarily drift feeders that infrequently
consume benthic organisms (Bachman 1984). Although it is possible that brown trout
altered the microhabitat use of some native fish species (e.g. Olson and Belk 2005), we
could not test for this effect with this data set.
Brown trout may also be affecting native fish in other ways that we were unable
to detect. Through size-selective predation, brown trout could alter the size structure of
native species (e.g. Nasmith et al. 2010), an effect we could not test for without fish
length data over time. Similarly, brown trout may be exploiting resources in such a way
that they affect the growth of resident native species, another effect that we could not
detect. Data sets that contain information on resident fish species before, during, and
after the invasion of brown trout are needed to address these effects.
The potential for brown trout to negatively affect native species may also depend
on other factors. Trout are thought to become piscivorous when they reach lengths of 130
mm to 160 mm (Mittelbach and Persson 1998), and others have reported strong effects of
brown trout on other species when suitable habitat is available and large (>150 mm)
brown trout are resident (McIntosh 2000; Olav Vik et al 2001). We did not consider
31
size-related effects of brown trout because fish length data from EMAP was not readily
accessible.
Considering our results together with evidence from other studies implies that
brown trout have variable effects on native species. We expected that the severity of the
effect brown trout have on natïve species may depend on either the type of taxa or
ecosystem exposed to brown trout (Figure 8, Table 6). For example, predation is thought
to be a common mechanism by which brown trout negatively affect native species.
However, as predominantly drift feeders (Bachman 1984), brown trout would be
expected to have negligible direct effects on those species associated with the streambed
or bottom of a lake compared with species that reside in the water column. This idea
appears to be too simplistic, though. Some bottom-oriented species have been severely
affected by brown trout (e.g. Arismendi et al 2009, Soto et al 2006), and some watercolumn oriented species are only moderately affected (e.g. Nasmith et al 2010).
In contrast, brown trout appear to more severely affect other salmonid species
than non-salmonid species (Figure 8), which implies that they more strongly affect
species with similar overall niches. Brown trout are considered more aggressive than
other salmonids (Nilsson 1963; Haswega et al. 2004), and some studies consider brown
trout to be a superior competitor than native salmonid species (Wang and White 1994;
Harwood et al. 2001; McHugh and Budy 2005, 2006; McHugh et al. 2008). In these
cases, brown trout may be acting as a novel competitor with native salmonid species for
either limited food or space resources.
32
Figure 8. Conceptual representation of the variable effects of brown trout on native
fishes. A small effect was inferred when a study did not detect any measureable effect, a
moderate effect (marked by the vertical line) was inferred as a measurable change that
still allowed the species to coexist with brown trout (in growth, habitat or diet selection),
and a large effect was inferred as a change in growth or survival that makes coexistence
with brown trout difficult or not possible. Benthic taxa are shown in bold font, and water
column species are shown in italics. Superscripts refer to the type of interaction:
a
predation, bcompetition, and cother. One species (*) was introduced to the native range
of brown trout. Subscripts identify the sources of information, which are given in Table
6.
To understand the overall effect of an introduced species, the specific interactions
thought to harm native species should be identified. In the case of brown trout,
competition for resources with native salmonids species has been demonstrated to
negatively affect those native species (Wang and White 1991; McHugh and Budy 2005,
2006). For native non-salmonid species, particularly potential prey species, these
interactions are less well defined and understood. While negative effects are often
assumed to be asymmetrical, results from other studies suggest that some non-salmonid
prey species can negatively affect brown trout through competition (e.g. Hesthagen and
Heggenes 2003).
33
Table 6. Sources used to construct Figure 8.
Effect Measured
Citation
1
growth, abundance
Nasmith 2010
2
habitat use
Olson and Belk 2005
3
diet composition
4
growth
Zimmerman 2005
Zimmerman and Vondracek
2006
5
growth
Ruetz et al. 2003
6
condition, growth
McHugh and Budy 2005
7
growth, diet composition, movement
McHugh and Budy 2006
8
biomass, presence/absence
Soto et al. 2006
9
1
0
1
1
1
2
1
3
1
4
1
5
1
6
1
7
1
8
presence/absence, distribution
Waters 1983
presence/absence, distribution
Moyle and Vondracek 1985
relative abundance
Arismendi et al. 2009
abundance
Garman and Nielsen 1982
biomass loss
Museth et al. 2003
habitat space
McIntosh et al. 1992
habitat use
L‟Abee-Lund et al. 1993
distribution
Townsend and Crowl 1991
abundance
Death and Death 2005
habitat use
Penaluna et al. 2009
34
It is also important to understand the spatial scale over which negative effects on
native species occur. The bulk of studies that consider the effects of brown trout on
native species have focused on local effects. These local studies reveal the potential
effects brown trout might have throughout its introduced range, but large-scale studies are
needed to assess regional impacts. The results of this study imply that brown trout may
not be having widespread negative effects on native aquatic vertebrate species in streams
of the western United States. Future work should focus on integrating local- and
regional-scale studies to better understand the environmental and ecological contexts that
lead to variable effects of introduced species such as brown trout on native species.
35
CHAPTER V
CONCLUSIONS
The introduction of exotic species is considered one of the greatest threats to
global biodiversity and the conservation of endangered species (Allan and Flecker 1993;
Sakai et al. 2001; Dudgeon et al. 2006). Exotic species have caused extirpations or
substantial reductions in native species abundance (Kitchell et al. 1997; McIntosh et al.
2010). But, it is widely held that of the many species introductions made annually, few
will result in successful establishment; and only some of those will result in severe
negative effects on the receiving ecosystem (Lodge 1993; Williamson 1996; Simberloff
2007). To develop appropriate management plans for any established exotic species, it is
important to understand how the magnitude of the effect that introduced species have
vary among ecosystems.
For my thesis, I used a data set that spanned a wide portion of the introduced
range of brown trout in North America to examine its effect on both individual prey
species and entire assemblages of aquatic vertebrates. I used data collected during the
EPA‟s Environmental Monitoring and Assessment Western Pilot Project that provided a
dataset that spanned a wide portion of the range of brown trout and native western United
States stream fish. Sites were located across the western United States and encompassed
a wide range of abiotic conditions. The methods I used to assess the effect of brown trout
on native taxa abundance and presence and absence provided easily interpretable results.
I used predictive modeling to examine if the likelihood of detecting two target taxa varied
36
with the presence of brown trout, a method that has previously been used to document
effects of brown trout on native species (Townsend and Crowl 1991). The lack of
association between native species and brown trout in this study compared with strong
negative associations observed elsewhere implies that the effect of brown trout on native
fishes may be contingent on the physical and biological structure of the area of interest.
In the rest of this chapter, I describe the context-dependent aspects of my study that may
have led to my results and outline future research needs.
The intent of this research was to determine if brown trout have severely affected
native fishes within a large portion of their introduced range. Although brown trout have
been shown to harm native stream fishes in individual watersheds or rivers (e.g. Garman
and Nielsen 1982; de la Hoz Franco and Budy 2005), the lack of any detected
relationship between native stream vertebrates and brown trout in this study suggests that
the presence of brown trout does not always cause negative effects.
Because brown trout are ecologically similar to native trout species, they may not
be performing an entirely novel function in western United States streams. Many native
non-salmonid fish species coexist with native piscivorous trout (e.g. cutthroat and
rainbow trout). Thus, the non-salmonid taxa I studied may already possess behaviors or
other traits that allow them to coexist with brown trout. In contrast, native trout are
probably highly vulnerable to introduced brown trout because of the high ecological
similarity among salmonid species that causes them to compete for resource with each
other (Waters 1983; McHugh and Budy 2005, 2005).
37
Although I did not observe negative effects of brown trout on other species in this
study, brown trout could be affecting native species in ways I could not detect. For
example, the effect of brown trout on native fishes has been shown to be size-dependent
(Garman and Nielsen 1982; McIntosh 2000). Large adult brown trout are considered to
be primarily piscivorous (Belica 2007), thereby making them potentially more dangerous
to prey species. Additionally, brown trout are gape-limited predators (Jensen et al. 2004),
so prey size may also affect the severity of the overall impact of brown trout on resident
native species. Despite the potential for size-related effects of brown trout, I was unable
to consider this relationship because I did not have length data for individual fish. In
addition, it is possible that although brown trout and native species occupy the same
reaches of streams, they use different microhabitats within those reaches. For example,
southern leatherside chub and juvenile mountain sucker in Utah occupied different
microhabitats in stream reaches that contained brown trout than others that did not
contain brown trout (Olson and Belk 2005). This effect was not detectable with the
EMAP dataset, however.
The current distribution and assemblage structure of western United States fishes
may represent a relative equilibrium between brown trout and native species. As
previously discussed, native species, such as sculpins, may already possess behaviors that
allow them to coexist with brown trout. Brown trout may have coexisted with other
native species for a sufficient amount of time for those species to evolve new antipredator
behaviors (e.g. 30 generations; O‟Steen et al. 2002). Additionally, brown trout may have
caused extirpations of other species, especially competitors, in some parts of the western
38
United States. A combination of these scenarios may explain the patterns observed in
native species assemblages and distributions in western United States streams.
I suggest that the reason that I did not detect a negative association between
brown trout and sculpins or speckled dace is due to the behaviors or adaptations that both
taxa possess that allows them to coexist with other piscivorous native trout species. It
would be useful to identify such behaviors or adaptations that facilitate such coexistence.
Studies that focus on areas where brown trout coexist with native species could help
identify such behaviors or other adaptations that allow this coexistence.
39
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